As the modern lifestyle and prevalence of chronic diseases have become a relevant issue of concern, functional food ingredients, nutraceuticals, and food supplements have become a significant area of research. Increasing sugar intake is of concern, because it may result in obesity, metabolic disorders, dental caries, and increased risk of noncommunicable diseases—hypertension, dyslipidemia, cardiovascular diseases, type 2 diabetes, cancer and others, which are responsible for more than half of all deaths worldwide [1
]. Possible harmful cardiometabolic mechanisms of action of dietary sugars include induction of inflammatory processes, oxidative stress, increasing insulin resistance, and impaired β-cell function [3
]. Sugars differ from each other in structure, effects, and applications. According to the structure, sugars can be referred to as: (1) Monosaccharides (glucose, fructose, and galactose), which have five or six carbon atoms, sweet taste and can be called reducing sugars; (2) disaccharides (sucrose, lactose, maltose, trehalose), which make up two or more monosaccharide units and may not have reducing properties; and (3) polyols—sugar alcohols (sorbitol, mannitol, lactitol, xylitol, erythritol, isomalt, maltitol). Sugars may naturally present in food or can be added to food additionally by the manufacturer or consumer. The latter is considered to be more dangerous because of the faster absorption and conversion to fats [4
Deleterious health effects may occur if sugars are consumed in large amounts [3
]. The same can be said about any macro- or micronutrient. The moderate intake of sugars, which according to WHO should be less than 10% of total energy intake, does not increase the health risk [1
]. While excessive amounts of sugars are undoubtedly unhealthy, rational use of sugars can be favorable. Sugars are a prominent constituent of plants, acting as structure matter and molecule signal, regulating growth and enzyme activity [7
]. Furthermore, they are the main energy source for the human body and an ubiquitous ingredient of our food, providing a desirable sweet taste [4
It has been suggested that some sugars take part in the anti-adherence activity. Adhesin proteins, fimbriae or pili, expose adhesive lectins on the cell surface, which bind complementary carbohydrates on the tissues of the host, and thus permit Escherichia coli
bacterial adhesion to the urothelium. Adhesin proteins can be mannose-resistant (p-fimbriae) or mannose-sensitive (type 1 fimbriae). The current hypothesis proposes that proanthocyanidins inhibit the adherence of p-fimbriae, and fructose inhibits adherence of type 1 fimbriae; consequently, uropathogenic bacteria cannot infect mucosal surface and postulate urinary tract infections [9
]. Hereby, fructose contributes to the disease-preventing properties of the most common bacterial infections, acquired in the community or hospitals [11
To avoid the harmful impact of sugars and to maintain their positive role, monitoring the concentration of sugars in food is needed, as well as choosing dietary sugars with low energy density that naturally occur in food—vegetables and fruits, including berries. According to this, lingonberries seem to be an appropriate source of dietary sugars [2
]. Lingonberry (Vaccinium vitis-idaea
L.) is a native plant to the boreal forest of North Eurasia and North America, nowadays generally accessible in most countries of Europe, especially in Scandinavia. Lingonberries can be consumed fresh, bought at the local markets, or cooked in the form of juices, jams, jellies, compotes, and syrups [12
]. These berries are widely used in the human diet, especially sweetened products, which are more favorable for most consumers [14
]. Fruits of this low-growing, evergreen shrub, belonging to the genus Vaccinium
L., are popular not only because of their unique taste, but also because of their high level of healthy bioactive compounds. Lingonberries are considered to be a good source of flavonols, anthocyanins, phenolic acids, proanthocyanidins, free amino acids, vitamins, omega-3 fatty acids, and minerals [15
]. A wide spectrum of biological activities of lingonberries has been determined. Lingonberries exhibit antimicrobial, anti-inflammatory, antioxidant, immunomodulatory, and antiproliferative activities and play a role in bacterial adhesion [12
]. Products of lingonberries are increasingly marketed as a natural solution for the treatment of various conditions, particularly urinary tract infections [18
However, the lingonberry’s composition and activity have not yet been fully investigated to date. Lingonberry is one of the least studied raw in the Ericaceae
family; besides that, most studies were conducted in the Nordic countries and focused mainly on phenolic compounds [19
]. Considering these berries’ popularity in food and health and wellness products, it is necessary to examine their sugar profile, due to potentially adverse effects. Lingonberries have historically been collected from the wild, and this is still mainly the case today. There are some cultivars produced, but there is no large-scale cultivation, and plant breeding of lingonberry is still in its infancy [20
]. Cultivation of lingonberry can best meet the increased needs of plant material. To optimize horticulturally important traits, evaluation the phytochemical differences between cultivated and wild lingonberries is needed, as well as emphasis of factors such as optimal collecting time and environmental conditions leading to better yield.
To the best of our knowledge, there have been no comprehensive studies on sugar analysis of many lingonberry coenopopulations, considering phenological growth stages, altitude, and latitude of the berries’ collecting locations. The variations of identified sugars have been presented for the first time for the cultivars and lower taxa. This is the first report on sugar composition of V. vitis-idaea var. leucocarpum, which is a unique white berry-bearing variety that is included in the National Genetic Resources of Lithuania. The obtained results will be really important to breeders for developing new cultivars and, of course, as a part of the ongoing interest in nutritional and nutraceutical properties of food, the content of sugars in lingonberries will be of interest to dietitians and may be used in the pharmaceutical industry in developing new products for consumers with special dietary requirements. Our results can contribute to quality improvement of lingonberry products, leading to increased acceptability of consumers and market size. The findings on the content of fructose in lingonberries may disclose the necessity of further studies on fructose from lingonberries as a natural anti-adhesive agent. The sugar profile and individual sugar ratio can also serve as a fruit authenticity tool to prevent adulterations.
Therefore, our aim was to characterize the sugar composition in wild clones from Lithuania, in seven cultivars (’Erntedank’, ’Erntekrone’, ’Kostromička’, ’Kostromskaja rozovaja’, ’Rubin’, ’Sanna’, ’Sussi’) and lower taxa (V. vitis-idaea var. leucocarpum) of lingonberries, considering genetic and environmental factors.
Lingonberries are described as very sour and quite tart berries with a little bit of sweetness. The flavor is very similar to cranberries. Organoleptic properties of lingonberries, like other fruits, are mainly determined by volatile compounds, sugars, organic acids, and their ratio [21
]. Since sugars in lingonberries affect consumer acceptability, a number of studies have been accomplished.
Mikulic-Petkovsek et al. analyzed various species of berries by the HPLC–RI method of analysis and detected glucose (37.9 ± 1.32 mg/g fresh weight (FW)), fructose (29.2 ± 0.71 mg/g FW), and sucrose (4.10 ± 0.45 mg/g FW) in wild lingonberries. Compared with other tested berries, the sugar level in lingonberries was just moderate. Similar contents of sugars were found in wild blackberries, red gooseberries, black mulberries, goji berries, and wild-grown elderberries [8
]. Almost the same amounts of sugars—up to 29, 36, and 2 mg/g FW of glucose, fructose, and sucrose, respectively—were determined earlier in lingonberries, bought from the local retail shop [22
]. The sugars were also found in the lingonberry juices, extracted with a hydraulic press. Viljakainen et al., by using the HPLC–RI method of analysis, found that amounts of fructose and glucose in Finnish lingonberry juices were almost equal (42.30 ± 0.27 and 42.38 ± 0.39 mg/mL, respectively) and contributed up to 98.6% of total sugars, whereas amounts of sucrose were very low (1.17 ± 0.01 mg/mL). Assessed amounts of total sugars were slightly higher in lingonberry juices than in juices of bilberry, cloudberry, blackcurrant, and strawberry, and almost two times higher than those of redcurrant, cranberry, and black crowberry [23
]. Recent studies have shown that sugars in lingonberry juices could be detected by a sensitive spectrophotometric method using enzymatic assay kits specific for these carbohydrates. It was proclaimed that squeezed lingonberry juices had 38.9 ± 0.43 mg/mL of fructose and 45.4 ± 0.71 mg/mL of glucose. Contents of sugars were similar to those of elderberry juices, but higher (p
< 0.05) than in cornelian cherry juices [24
]. One more report revealed that bioprocessing unaffected, fully riped Finnish lingonberries accumulated high amounts of fructose (260 ± 0.01 mg/g DW), glucose (248 ± 0.03 mg/g DW), and sucrose (23.0 ± 0.01 mg/g DW) [21
Our determined sugar amounts might seem higher than in previous studies, except the latter one, in which observed sugar composition was consistent with the results of the present study. It can be explained that in all of the researches mentioned above, except the latter one, the results were expressed for fresh raw material, meanwhile in ours for dry raw material (lyophilized lingonberries). The differences in contents of sugars also can be attributed primarily to the morphotype of lingonberries, as well as geographical locations, prevailing climatic conditions, fruit ripeness, their collecting date, and diversity of processing, extraction, and sugar analysis.
Notwithstanding the distinctions between sugar concentrations, contributions of fructose, glucose, and sucrose of total sugars were partly consistent in previous studies, and a number of reports proved that the main sugars of lingonberries are fructose and glucose. The amounts of other sugar components could appear only after hydrolysis of polysaccharide fraction. Ross et al., by using gas–liquid chromatography with FID detector, found impressively high amounts of arabinose, xylose, and galactose, and lower amounts of mannose, fucose, and rhamnose in water-extractable polysaccharides fraction from Northern Manitoba lingonberries [25
]. Some of these sugars were looked at in the present study as well, but results showed that they cannot be found in lingonberries as free sugars.
Results of the present study and literature data revealed that sugar concentration in lingonberries is higher than in the most popular berries, like bilberries, strawberries, and cranberries. However, the sweet taste is hidden because of the high organic acid content. Several studies have shown that lingonberries accumulate high amounts of citric, fumaric, and shikimic, and lower amounts of tartaric, benzoic and malic acids, which result in pH decreasing of lingonberries [8
]. Bioprocessing of lingonberries with enzymes, lactic acid bacterias, yeast, or their combination has an important impact on sugars composition, and enzyme treatment could be a potential tool for decreasing the acidic flavor of lingonberries [21
It is acknowledged that lingonberries are indigenous to the sandy, northern, temperate, boreal forests; they prefer light and well-drained, porous, acidic (pH range between 4.3 and 5.5) soils. However, lingonberries are not demanding—they are resistant to temperature fluctuations, require very little water, and can grow in very different habitats within its extensive natural range, from dry oligotrophic pinewoods to raised bogs [26
]. Lithuanian boreal forests seem to be a suitable place for the growth of lingonberries. Considering the sugar amounts in lingonberries from different collecting locations of Lithuania, it was noticed that the amounts of sugars in medium humidity, very infertile, pine tree with full sun or partial shade forests (e.g., Varėna, Valkininkai, Aukštadvaris, Marcinkonys) were higher (p
< 0.05) than in medium humidity, medium fertility, with large variety of tree species shaded forests (e.g., Gineitiškės, Jurašiškės). Thus, our results are in accordance with the literature data and indicate that lingonberries accumulate higher amounts of compounds in sunny, dry tree sites, and even very infertile land can be a great growth place for lingonberries. Detailed studies are needed on the accumulation of other bioactive compounds in different soils, determining the organic and mineral composition of the soil.
Our determined amounts of sugars in different cultivars of lingonberries were partly consistent with their description of the flavors and yield. Cultivars in which berries are characterized as weakly acidic or sweet-and-sour in taste were distinguished by the highest amounts of sugars (‘Erntedank’, ‘Sussi’, ‘Kostromička’, which were attributed to the same cluster, and ‘Ertekrone’, which was attributed to a separate cluster). Meanwhile, the cultivars in which berries are described as having a sour taste and producing poor fall crop accumulated the lowest amounts of fructose and glucose (‘Sanna’ and ‘Rubin’, which were attributed to the same cluster) [26
The composition of bioactive compounds in cultivated lingonberries is the subject of numerous studies. Lee et al. analyzed five different cultivars, including Swedish cultivars ‘Sanna’ and ‘Sussi’, which were also examined in our study. They assessed that lingonberries of these cultivars accumulated the lowest (p
< 0.05) amounts of amino acids and moderate amounts of anthocyanins, total phenolics, and total tannins [13
]. The lowest sugar productivity by ‘Sanna’ and one of the highest by ‘Sussi’ was observed in the present material. Phenolic compounds from lingonberry leaves within the same cultivars and lower taxa as in the present study were investigated previously by us. The greatest amounts of phenolics were found in the leaf extracts from ‘Rubin’ and ‘Kostromskaja rozovaja’ cultivars, whereas the lowest ones in ‘Erntedank’, ‘Erntesegen’, and ‘Sanna’ cultivars. The cluster analysis revealed that, according to the composition of phenolic compounds, the clusters were related to the countries of origin, especially with German and Russian origin cultivars [30
]. According to the present findings, ‘Rubin’ and ‘Kostromskaja rozovaja’ cultivars accumulated just moderate amounts of sugars in berries, ‘Sanna’ with the lowest (p
< 0.05), and ‘Erntedank’, ‘Erntesegen’ with the highest ones. Furthermore, there was no link between the cultivar country of origin and the quantities of sugars in berries. Contents of sugars do not seem to correlate with the contents of other compounds in the same cultivars and lower taxa of lingonberries. The productivity of cultivars in terms of sugars and in terms of other compounds is probably different. However, it is hard to compare the results from the earlier and present study, because of the different studied cultivars or raw materials.
Taking into account the importance of genetic differences and control of cultivation conditions, it is anticipated that amounts of bioactive compounds should be different among wild clones and cultivated plants. Notwithstanding, we found that there were no statistically significant differences in sugar amounts between cultivated and wild lingonberries. Several researchers found higher levels of phenolic compounds in wild fruits, meanwhile, the concentration of total sugars was quite similar between cultivated and wild fruits, as in our study [8
]. This information could be relevant for breeders that are interested in sugar levels in the development of new cultivars, and it indicates that they should look at some other cultivation techniques that may help affect the sugar content. The successful development of lingonberry cultivars would increase the market size.
Altitude and latitude of location have an impact on temperature and solar radiation. As the latitude of a location increases, it receives less sunlight, whereas increasing altitude results in a decrease in pressure and thus in temperature. It is anticipated that most plants may adapt to higher latitudes and altitudes. Harsh weather conditions could affect processes associated with plant development and significantly enhance the biosynthesis of bioactive compounds [33
]. Vyas et al. determined that amounts of secondary metabolites—anthocyanins, proanthocyanidins, and total antioxidant activity—of wild lingonberries positively correlated with latitude and altitude of the berries’ collecting locations [35
]. Our study showed contrary results—higher altitude and latitude, less sunlight and lower temperature reduced sugar production in lingonberries. Consequently, we suggest that the synthesis of primary metabolites does not intensify under the harsh weather conditions.
The variability and contents of bioactive compounds in plants depend on many factors, such as the already discussed genetic and environmental factors, cultivation conditions, processing, extraction method, and also maturity stage [36
]. Numerous studies have been conducted to determine the amounts of bioactive compounds in various berries during the growing season, thus finding out the optimal collecting time [36
]. Hence, we figured out that the changes in the sugar levels during the growing season were apparent in lingonberries and the highest amounts accumulated at the end of the vegetation. So, late September would be the optimal collecting time for those who prefer sweeter berries. Analysis of the relationship of sugar amounts in lingonberries and consumer expectations would help to develop the best quality standards for collecting dates.
Although there are considerable amounts of sugars in lingonberries, there is no need to worry about high sugar intake with these berries leading to deleterious health effects. These effects may occur if only more than about 1.25 kg of fresh lingonberries would be eaten daily, and more than 2.5 kg/day of fresh lingonberries would contribute to weight gain [6
]. Meanwhile, the moderate intake of lingonberries may trigger satiety and promote a positive energy balance due to sugars; also lingonberry inclusion in the diet predisposes prevention of various human chronic diseases, because of the richness of the phenolic antioxidants [39
]. Published papers show the potential benefit of lingonberries against diabetes and hypertension. These berries can inhibit α-amylase, α-glucosidase, anti-diabetic agent acarbose, and significantly enhance glucose uptake in human liver cells, decreasing glycemia and insulin levels [40
]. Kivimäki et al. reported that lingonberry juices at small concentrations affect plasma inflammatory markers, clinical chemistry variables, and may lower blood pressure in long-term treatment [42
]. Furthermore, lingonberry extracts with strong antioxidant function consumed orally or topically can protect dermal collagen protein, reduce the production and activity of elastinase, relieve skin wrinkles and colored spots, and thus improve skin conditions [43
]. Therefore, products of lingonberries are promising beauty and health therapeutic candidates in the cosmetic and pharmaceutical industries.